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Restraint stress of male mice triggers apoptosis in spermatozoa and spermatogenic cells via activating the TNF-α system

Published online by Cambridge University Press:  14 January 2020

Jie Zhang ,
De-Ling Kong ,
Bin Xiao ,
Hong-Jie Yuan ,
Qiao-Qiao Kong ,
Xiao Han ,
Ming-Jiu Luo  and
Jing-He Tan Open the ORCID record for Jing-He Tan [Opens in a new window]
Jie Zhang
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City271018, People’s Republic of China
De-Ling Kong
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City271018, People’s Republic of China
Bin Xiao
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City271018, People’s Republic of China
Hong-Jie Yuan
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City271018, People’s Republic of China
Qiao-Qiao Kong
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City271018, People’s Republic of China
Xiao Han
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City271018, People’s Republic of China
Ming-Jiu Luo*
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City271018, People’s Republic of China
Jing-He Tan*
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City271018, People’s Republic of China
*
Author for correspondence: Jing-He Tan or Ming-Jiu Luo, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai-an City, Shandong Province271018, People’s Republic of China. Tel: +86 538 8249616. Fax: +86 538 8241419. E-mail: [email protected] or [email protected]
Author for correspondence: Jing-He Tan or Ming-Jiu Luo, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai-an City, Shandong Province271018, People’s Republic of China. Tel: +86 538 8249616. Fax: +86 538 8241419. E-mail: [email protected] or [email protected]
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Summary

Studies have indicated that psychological stress impairs human fertility and that various stressors can induce apoptosis of testicular cells. However, the mechanisms by which psychological stress on males reduces semen quality and stressors induce apoptosis in testicular cells are largely unclear. Using a psychological (restraint) stress mouse model, we tested whether male psychological stress triggers apoptosis of spermatozoa and spermatogenic cells through activating tumour necrosis factor (TNF)-α signalling. Wild-type or TNF-α−/− male mice were restrained for 48 h before examination for apoptosis and expression of TNF-α and TNF receptor 1 (TNFR1) in spermatozoa, epididymis, seminiferous tubules and spermatogenic cells. The results showed that male restraint significantly decreased fertilization rate and mitochondrial membrane potential, while increasing levels of malondialdehyde, active caspase-3, TNF-α and TNFR1 in spermatozoa. Male restraint also increased apoptosis and expression of TNF-α and TNFR1 in caudae epididymides, seminiferous tubules and spermatogenic cells. Sperm quality was also significantly impaired when spermatozoa were recovered 35 days after male restraint. The restraint-induced damage to spermatozoa, epididymis and seminiferous tubules was significantly ameliorated in TNF-α−/− mice. Furthermore, incubation with soluble TNF-α significantly reduced sperm motility and fertilizing potential. Taken together, the results demonstrated that male psychological stress induces apoptosis in spermatozoa and spermatogenic cells through activating the TNF-α system and that the stress-induced apoptosis in spermatogenic cells can be translated into impaired quality in future spermatozoa.

Keywords

ApoptosisPsychological stressSemen qualitySpermatogenesisTNF-α signalling
Type
Research Article
Information
Zygote , Volume 28 , Issue 2 , April 2020 , pp. 160 - 169
Copyright
© Cambridge University Press 2020

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Footnotes

*

Jie Zhang and De-Ling Kong contributed equally to this work.

References

Adedara, IA, Oyebiyi, OO, Lawal, TA, Adesina, AA and Farombi, EO (2013) Involvement of oxidative stress in municipal landfill leachate-induced toxicity in boar sperm. Environ Toxicol Pharmacol 36, 972–8.CrossRefGoogle ScholarPubMed
Aitken, RJ and Baker, MA (2013) Causes and consequences of apoptosis in spermatozoa; contributions to infertility and impacts on development. Int J Dev Biol 57, 265–72.CrossRefGoogle ScholarPubMed
Aitken, RJ, De Iuliis, GN, Gibb, Z and Baker, MA (2012) The Simmet lecture: new horizons on an old landscape--oxidative stress, DNA damage and apoptosis in the male germ line. Reprod Domest Anim 47(Suppl 4), 7–14.CrossRefGoogle ScholarPubMed
Białas, M, Fiszer, D, Rozwadowska, N, Kosicki, W, Jedrzejczak, P and Kurpisz, M (2009) The role of IL-6, IL-10, TNF-alpha and its receptors TNFR1 and TNFR2 in the local regulatory system of normal and impaired human spermatogenesis. Am J Reprod Immunol 62, 51–9.CrossRefGoogle ScholarPubMed
Boekelheide, K, Lee, J, Shipp, EB, Richburg, JH and Li, G (1998) Expression of Fas system-related genes in the testis during development and after toxicant exposure. Toxicol Lett 102–103, 503–8.CrossRefGoogle ScholarPubMed
Cho, J and Lee, DG (2011) Oxidative stress by antimicrobial peptide pleurocidin triggers apoptosis in Candida albicans. Biochimie 93, 1873–9.CrossRefGoogle ScholarPubMed
Collodel, G, Moretti, E, Fontani, V, Rinaldi, S, Aravagli, L, Saragò, G, Capitani, S and Anichini, C (2008) Effect of emotional stress on sperm quality. Indian J Med Res 128, 254–61.Google ScholarPubMed
Cottet-Rousselle, C, Ronot, X, Leverve, X and Mayol, JF (2011) Cytometric assessment of mitochondria using fluorescent probes. Cytometry A 79, 405–25.CrossRefGoogle ScholarPubMed
Dacheux, JL and Dacheux, F (2013) New insights into epididymal function in relation to sperm maturation. Reproduction 147, R27–42.CrossRefGoogle ScholarPubMed
De, SK, Chen, HL, Pace, JL, Hunt, JS, Terranova, PF and Enders, GC (1993) Expression of tumour necrosis factor-alpha in mouse spermatogenic cells. Endocrinology 133, 389–96.CrossRefGoogle ScholarPubMed
Dhanabalan, S, D’Cruz, SC and Mathur, PP (2010) Effects of corticosterone and 2,3,7,8-tetrachloro-dibenzo-p-dioxin on epididymal antioxidant system in adult rats. J Biochem Mol Toxicol 24, 242–9.CrossRefGoogle ScholarPubMed
Dhanabalan, S, Jubendradass, R, Latha, P and Mathur, PP (2011) Effect of restraint stress on 2,3,7,8 tetrachloro dibenzo-p-dioxin induced testicular and epididymal toxicity in rats. Hum Exp Toxicol 30, 567–78.CrossRefGoogle ScholarPubMed
Estrada, LS, Champion, HC, Wang, R, Rajasekaran, M, Hellstrom, WJ, Aggarwal, B and Sikka, SC (1997) Effect of tumour necrosis factor-alpha (TNF-α) and interferon-gamma (IFN-gamma) on human sperm motility, viability and motion parameters. Int J Androl 20, 237–42.CrossRefGoogle ScholarPubMed
Fenster, L, Katz, DF, Wyrobek, AJ, Pieper, C, Rempel, DM, Oman, D snd Swan, SH (1997) Effects of psychological stress on human semen quality. J Androl 18, 194–202.Google ScholarPubMed
Glavin, GB, Paré, WP, Sandbak, T, Bakke, HK and Murison, R (1994) Restraint stress in biomedical research: an update. Neurosci Biobehav Rev 18, 223–49.CrossRefGoogle ScholarPubMed
Gollenberg, AL, Liu, F, Brazil, C, Drobnis, EZ, Guzick, D, Overstreet, JW, Redmon, JB, Sparks, A, Wang, C and Swan, SH (2010) Semen quality in fertile men in relation to psychosocial stress. Fertil Steril 93, 1104–11.CrossRefGoogle ScholarPubMed
Heiskanen, KM, Bhat, MB, Wang, HW, Ma, J and Nieminen, AL (1999) Mitochondrial depolarization accompanies cytochrome c release during apoptosis in PC6 cells. J Biol Chem 274, 5654–8.CrossRefGoogle ScholarPubMed
Hristov, G, Marttila, T, Durand, C, Niesler, B, Rappold, GA and Marchini, A (2014) SHOX triggers the lysosomal pathway of apoptosis via oxidative stress. Hum Mol Genet 23, 1619–30.CrossRefGoogle ScholarPubMed
Janevic, T, Kahn, LG, Landsbergis, P, Cirillo, PM, Cohn, BA, Liu, X and Factor-Litvak, P (2014) Effects of work and life stress on semen quality. Fertil Steril 102, 530–8.CrossRefGoogle ScholarPubMed
Kavurma, MM, Tan, NY and Bennett, MR (2008) Death receptors and their ligands in atherosclerosis. Arterioscler Thromb Vasc Biol 28, 1694–702.CrossRefGoogle ScholarPubMed
Koji, T, Hishikawa, Y, Ando, H, Nakanishi, Y and Kobayashi, N (2001) Expression of Fas and Fas ligand in normal and ischemia-reperfusion testes: involvement of the Fas system in the induction of germ cell apoptosis in the damaged mouse testis. Biol Reprod 64, 946–54.CrossRefGoogle ScholarPubMed
Lampiao, F and du Plessis, SS (2008) TNF-alpha and IL-6 affect human sperm function by elevating nitric oxide production. Reprod Biomed Online 17, 628–31.CrossRefGoogle ScholarPubMed
Liu, T, Zhong, S, Liao, X, Chen, J, He, T, Lai, S and Jia, Y (2015) A meta-analysis of oxidative stress markers in depression. PLoS One 10, e0138904.CrossRefGoogle ScholarPubMed
Lu, WC, Wang, AQ, Chen, XL, Yang, G, Lin, Y, Chen, YO, Hong, CJ and Tian, HL (2014) 90d exposure to nonylphenol has adverse effects on the spermatogenesis and sperm maturation of adult male rats. Biomed Environ Sci 27, 907–11.Google ScholarPubMed
Lysiak, JJ (2004) The role of tumour necrosis factor-alpha and interleukin-1 in the mammalian testis and their involvement in testicular torsion and autoimmune orchitis. Reprod Biol Endocrinol 2, 9.CrossRefGoogle ScholarPubMed
Miura, M, Sasagawa, I, Suzuki, Y, Nakada, T and Fujii, J (2002) Apoptosis and expression of apoptosis-related genes in the mouse testis following heat exposure. Fertil Steril 77, 787–93.CrossRefGoogle ScholarPubMed
Moazamian, R, Polhemus, A, Connaughton, H, Fraser, B, Whiting, S, Gharagozloo, P and Aitken, RJ (2015) Oxidative stress and human spermatozoa: diagnostic and functional significance of aldehydes generated as a result of lipid peroxidation. Mol Hum Reprod 21, 502–15.CrossRefGoogle ScholarPubMed
Moore, HD (1998) Contribution of epididymal factors to sperm maturation and storage. Andrologia 30, 233–9.CrossRefGoogle ScholarPubMed
Nargund, VH (2015) Effects of psychological stress on male fertility. Nat Rev Urol 12, 373–82.CrossRefGoogle ScholarPubMed
Oakberg, EF (1956) Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am J Anat 99, 507–16.CrossRefGoogle ScholarPubMed
Oh, YS, Na, EJ and Gye, MC (2016) Effects of bilateral vasectomy on the interleukin 1 system in mouse epididymis. Am J Reprod Immunol 76, 235–42.CrossRefGoogle ScholarPubMed
Paré, WP and Glavin, GB (1986) Restraint stress in biomedical research: a review. Neurosci Biobehav Rev 10, 339–70.CrossRefGoogle ScholarPubMed
Payan-Carreira, R, Santana, I, Pires, MA, Holst, BS and Rodriguez-Martinez, H (2012) Localization of tumour necrosis factor in the canine testis, epididymis and spermatozoa. Theriogenology 77, 1540–8.CrossRefGoogle ScholarPubMed
Pérez-Crespo, M, Pintado, B and Gutiérrez-Adán, A (2008) Scrotal heat stress effects on sperm viability, sperm DNA integrity, and the offspring sex ratio in mice. Mol Reprod Dev 75, 40–7.CrossRefGoogle ScholarPubMed
Rahman, MB, Schellander, K, Luceño, NL and Van Soom, A (2018) Heat stress responses in spermatozoa: mechanisms and consequences for cattle fertility. Theriogenology 113, 102–12.CrossRefGoogle ScholarPubMed
Sasagawa, I, Yazawa, H, Suzuki, Y and Nakada, T (2001) Stress and testicular germ cell apoptosis. Arch Androl 47, 211–6.CrossRefGoogle ScholarPubMed
Siervo, GEML, Ogo, FM, Valério, AD, Silva, TNX, Staurengo-Ferrari, L, Alvarenga, TA, Cecchini, R, Verri, WA, Guarnier, FA, Andersen, ML and Fernandes, GSA (2017) Sleep restriction in Wistar rats impairs epididymal postnatal development and sperm motility in association with oxidative stress. Reprod Fertil Dev 29, 1813–20.CrossRefGoogle ScholarPubMed
Smiley, ST, Reers, M, Mottola-Hartshorn, C, Lin, M, Chen, A, Smith, TW, Steele, GD Jr and Chen, LB (1991) Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc Natl Acad Sci USA 88, 3671–5.CrossRefGoogle ScholarPubMed
Suescun, MO, Rival, C, Theas, MS, Calandra, RS and Lustig, L (2003) Involvement of tumour necrosis factor-alpha in the pathogenesis of autoimmune orchitis in rats. Biol Reprod 68, 2114–21.CrossRefGoogle ScholarPubMed
Wu, XF, Yuan, HJ, Li, H, Gong, S, Lin, J, Miao, YL, Wang, TY and Tan, JH (2015) Restraint stress on female mice diminishes the developmental potential of oocytes: roles of chromatin configuration and histone modification in germinal vesicle stage oocytes. Biol Reprod 92, 13.CrossRefGoogle ScholarPubMed
Wu, YT, Wu, SB and Wei, YH (2014) Metabolic reprogramming of human cells in response to oxidative stress: implications in the pathophysiology and therapy of mitochondrial diseases. Curr Pharm Des 20, 5510–26.CrossRefGoogle ScholarPubMed
Xiao, B, Li, X, Feng, XY, Gong, S, Li, ZB, Zhang, J, Yuan, HJ and Tan, JH (2019) Restraint stress of male mice induces apoptosis in spermatozoa and spermatogenic cells: role of the FasL/Fas system. Biol Reprod 101, 235–47.CrossRefGoogle Scholar
Yazawa, H, Sasagawa, I, Ishigooka, M and Nakada, T (1999) Effect of immobilization stress on testicular germ cell apoptosis in rats. Hum Reprod 14, 1806–10.CrossRefGoogle ScholarPubMed
Zhang, SY, Wang, JZ, Li, JJ, Wei, DL, Sui, HS, Zhang, ZH, Zhou, P and Tan, JH (2011) Maternal restraint stress diminishes the developmental potential of oocytes. Biol Reprod 84, 672–81.CrossRefGoogle ScholarPubMed
Zhao, LH, Cui, XZ, Yuan, HJ, Liang, B, Zheng, LL, Liu, YX, Luo, MJ and Tan, JH (2013) Restraint stress inhibits mouse implantation: temporal window and the involvement of HB-EGF, estrogen and progesterone. PLoS One 8, e80472.CrossRefGoogle ScholarPubMed